Systematic imaging in medicine: a comprehensive review

Abstract

Systematic imaging can be broadly defined as the systematic identification and characterization of biological processes at multiple scales and levels. In contrast to “classical” diagnostic imaging, systematic imaging emphasizes on detecting the overall abnormalities including molecular, functional, and structural alterations occurring during disease course in a systematic manner, rather than just one aspect in a partial manner. Concomitant efforts including improvement of imaging instruments, development of novel imaging agents, and advancement of artificial intelligence are warranted for achievement of systematic imaging. It is undeniable that scientists and radiologists will play a predominant role in directing this burgeoning field. This article introduces several recent developments in imaging modalities and nanoparticles-based imaging agents, and discusses how systematic imaging can be achieved. In the near future, systematic imaging which combines multiple imaging modalities with multimodal imaging agents will pave a new avenue for comprehensive characterization of diseases, successful achievement of image-guided therapy, precise evaluation of therapeutic effects, and rapid development of novel pharmaceuticals, with the final goal of improving human health-related outcomes.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Weissleder R, Mahmood U. Molecular imaging. Radiology. 2001;219(2):316–33. https://doi.org/10.1148/radiology.219.2.r01ma19316.

    CAS  PubMed  Article  Google Scholar 

  2. 2.

    Antaris AL, Chen H, Cheng K, Sun Y, Hong G, Qu C, et al. A small-molecule dye for NIR-II imaging. Nat Mater. 2016;15(2):235–42. https://doi.org/10.1038/nmat4476.

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Lheureux S, Denoyelle C, Ohashi PS, De Bono JS, Mottaghy FM. Molecularly targeted therapies in cancer: a guide for the nuclear medicine physician. Eur J Nucl Med Mol Imaging. 2017;44(Suppl 1):41–54. https://doi.org/10.1007/s00259-017-3695-3.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Taniwaki M, Windecker S, Raber L. Silent myocardial infarction and stroke: findings of multimodality imaging. Eur Heart J. 2014;36(16):949. https://doi.org/10.1093/eurheartj/ehu477.

    PubMed  Article  Google Scholar 

  5. 5.

    Chen IY, Wu JC. Cardiovascular molecular imaging: focus on clinical translation. Circulation. 2011;123(4):425–43. https://doi.org/10.1161/CIRCULATIONAHA.109.916338.

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Slifstein M, van de Giessen E, Van Snellenberg J, Thompson JL, Narendran R, Gil R, et al. Deficits in prefrontal cortical and extrastriatal dopamine release in schizophrenia: a positron emission tomographic functional magnetic resonance imaging study. JAMA Psychiatry. 2015;72(4):316–24. https://doi.org/10.1001/jamapsychiatry.2014.2414.

    PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Chalela JA, Kidwell CS, Nentwich LM, Luby M, Butman JA, Demchuk AM, et al. Magnetic resonance imaging and computed tomography in emergency assessment of patients with suspected acute stroke: a prospective comparison. Lancet. 2007;369(9558):293–8. https://doi.org/10.1016/s0140-6736(07)60151-2.

    PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372(11):1009–18. https://doi.org/10.1056/NEJMoa1414792.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Hammoud DA. Molecular imaging of inflammation: current status. J Nucl Med. 2016;57(8):1161–5. https://doi.org/10.2967/jnumed.115.161182.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Signore A, Mather S, Piaggio G, Malviya G, Dierckx R. Molecular imaging of inflammation/infection: nuclear medicine and optical imaging agents and methods. Chem Rev. 2010;110(5):3112–45. https://doi.org/10.1021/cr900351r.

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Santangelo PJ, Rogers KA, Zurla C, Blanchard EL, Gumber S, Strait K, et al. Whole-body immunoPET reveals active SIV dynamics in viremic and antiretroviral therapy-treated macaques. Nat Methods. 2015;12(5):427–32. https://doi.org/10.1038/nmeth.3320.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. 12.

    Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS, Vale RD. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell. 2014;159(3):635–46. https://doi.org/10.1016/j.cell.2014.09.039.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Louie AY, Hüber MM, Ahrens ET, Rothbächer U, Moats R, Jacobs RE, et al. In vivo visualization of gene expression using magnetic resonance imaging. Nat Biotechnol. 2000;18(3):321–5. https://doi.org/10.1038/73780.

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Segal E, Sirlin CB, Ooi C, Adler AS, Gollub J, Chen X, et al. Decoding global gene expression programs in liver cancer by noninvasive imaging. Nat Biotechnol. 2007;25(6):675–80. https://doi.org/10.1038/nbt1306.

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Van Roessel P, Brand AH. Imaging into the future: visualizing gene expression and protein interactions with fluorescent proteins. Nat Cell Biol. 2002;4(1):E15. https://doi.org/10.1038/ncb0102-e15.

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Willmann JK, van Bruggen N, Dinkelborg LM, Gambhir SS. Molecular imaging in drug development. Nat Rev Drug Discov. 2008;7(7):591–607. https://doi.org/10.1038/nrd2290.

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Seemann MD, Nekolla S, Ziegler S, Bengel F, Schwaiger M. PET/CT: fundamental principles. Eur J Med Res. 2004;9(5):241–6.

    PubMed  Google Scholar 

  18. 18.

    Cherry SR, Badawi RD, Karp JS, Moses WW, Price P, Jones T. Total-body imaging: transforming the role of positron emission tomography. Sci Transl Med. 2017;9(381):eaaf6169. https://doi.org/10.1126/scitranslmed.aaf6169.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Pelc NJ, Kinahan PE, Pettigrew RI. Special section guest editorial: positron emission tomography: history, current status, and future prospects. J Med Imaging. 2017;4(1). https://doi.org/10.1117/1.JMI.4.1.011001.

  20. 20.

    Jung JH, Choi Y, Im KC. PET/MRI: technical challenges and recent advances. Nucl Med Mol Imaging. 2016;50(1):3–12. https://doi.org/10.1007/s13139-016-0393-1.

    PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Brix G, Lechel U, Glatting G, Ziegler SI, Münzing W, Müller SP, et al. Radiation exposure of patients undergoing whole-body dual-modality 18F-FDG PET/CT examinations. J Nucl Med. 2005;46(4):608–13.

    CAS  PubMed  Google Scholar 

  22. 22.

    Afaq A, Syed R, Bomanji J. PET/MRI: a new technology in the field of molecular imaging. Br Med Bull. 2013;108:159–71. https://doi.org/10.1093/bmb/ldt032.

    PubMed  Article  Google Scholar 

  23. 23.

    Ko GB, Yoon HS, Kim KY, Lee MS, Yang BY, Jeong JM, et al. Simultaneous multiparametric PET/MRI with silicon photomultiplier PET and ultra-high-field MRI for small-animal imaging. J Nucl Med. 2016;57(8):1309–15. https://doi.org/10.2967/jnumed.115.170019.

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    Xie WH, Zhang B, Wang LH, Liu CY, Chang C, Lei B, et al. Biodistribution characteristics and SPECT imaging of (99 m)Tc-RET and (99 m)Tc-REG in human lung cancer xenografts. Cancer Biother Radiopharm. 2015;30(3):117–24. https://doi.org/10.1089/cbr.2014.1765.

    CAS  PubMed  Article  Google Scholar 

  25. 25.

    Li F, Cheng T, Dong Q, Wei R, Zhang Z, Luo D, et al. Evaluation of 99mTc-HYNIC-TMTP1 as a tumor-homing imaging agent targeting metastasis with SPECT. Nucl Med Biol. 2015;42(3):256–62. https://doi.org/10.1016/j.nucmedbio.2014.11.001.

    CAS  PubMed  Article  Google Scholar 

  26. 26.

    Clark DP, Badea C. Micro-CT of rodents: state-of-the-art and future perspectives. Phys Med. 2014;30(6):619–34. https://doi.org/10.1016/j.ejmp.2014.05.011.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Metscher BD. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol. 2009;9:11. https://doi.org/10.1186/1472-6793-9-11.

    PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Zhang Z, Yu S, Liang X, Zhu Y, Xie Y. A novel design of ultrafast micro-CT system based on carbon nanotube: a feasibility study in phantom. Phys Med. 2016;32(10):1302–7. https://doi.org/10.1016/j.ejmp.2016.06.016.

    PubMed  Article  Google Scholar 

  29. 29.

    Shin D, Pierce MC, Gillenwater AM, Williams MD, Richards-Kortum RR. A fiber-optic fluorescence microscope using a consumer-grade digital camera for in vivo cellular imaging. PLoS One. 2010;5(6):e11218. https://doi.org/10.1371/journal.pone.0011218.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Miyamoto D, Murayama M. The fiber-optic imaging and manipulation of neural activity during animal behavior. Neurosci Res. 2016;103:1–9. https://doi.org/10.1016/j.neures.2015.09.004.

    PubMed  Article  Google Scholar 

  31. 31.

    Caucheteur C, Guo T, Albert J. Review of plasmonic fiber optic biochemical sensors: improving the limit of detection. Anal Bioanal Chem. 2015;407(14):3883–97. https://doi.org/10.1007/s00216-014-8411-6.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Muldoon TJ, Anandasabapathy S, Maru D, Richards-Kortum R. High-resolution imaging in Barrett's esophagus: a novel, low-cost endoscopic microscope. Gastrointest Endosc. 2008;68(4):737–44. https://doi.org/10.1016/j.gie.2008.05.018.

    PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Muldoon TJ, Pierce MC, Nida DL, Williams MD, Gillenwater A, Richards-Kortum R. Subcellular-resolution molecular imaging within living tissue by fiber microendoscopy. Opt Express. 2007;15(25):16413–23. https://doi.org/10.1364/oe.15.016413.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. 34.

    Camirand G. New perspectives in transplantation through intravital microscopy imaging. Curr Opin Organ Transplant. 2013;18(1):6–12. https://doi.org/10.1097/MOT.0b013e32835c96c6.

    PubMed  Article  Google Scholar 

  35. 35.

    Gavins FN. Intravital microscopy: new insights into cellular interactions. Curr Opin Pharmacol. 2012;12(5):601–7. https://doi.org/10.1016/j.coph.2012.08.006.

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Sharaf R, Mempel TR, Murooka TT. Visualizing the behavior of hiv-infected t cells in vivo using multiphoton intravital microscopy. Methods Mol Biol. 2016;1354:189–201. https://doi.org/10.1007/978-1-4939-3046-3_13.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. 37.

    Liang HD, Blomley MJ. The role of ultrasound in molecular imaging. Br J Radiol. 2003;76(Spec No 2):S140-50. https://doi.org/10.1259/bjr/57063872.

  38. 38.

    He X, Wu DF, Ji J, Ling WP, Chen XL, Chen YX. Ultrasound microbubble-carried PNA targeting to c-myc mRNA inhibits the proliferation of rabbit iliac arterious smooth muscle cells and intimal hyperplasia. Drug Deliv. 2016;23(7):2482–7. https://doi.org/10.3109/10717544.2015.1014947.

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Spivak I, Rix A, Schmitz G, Fokong S, Iranzo O, Lederle W, et al. Low-dose molecular ultrasound imaging with e-selectin-targeted PBCA microbubbles. Mol Imaging Biol. 2015;18(2):180–90. https://doi.org/10.1007/s11307-015-0894-9.

    CAS  Article  Google Scholar 

  40. 40.

    Sharpe J. Optical projection tomography. Annu Rev Biomed Eng. 2004;6:209–28. https://doi.org/10.1146/annurev.bioeng.6.040803.140210.

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Quintana L, Sharpe J. Optical projection tomography of vertebrate embryo development. Cold Spring Harb Protoc. 2011;2011(6):586–94. https://doi.org/10.1101/pdb.top116.

    PubMed  Article  Google Scholar 

  42. 42.

    Singh M, Raghunathan R, Piazza V, Davis-Loiacono AM, Cable A, Vedakkan TJ, et al. Applicability, usability, and limitations of murine embryonic imaging with optical coherence tomography and optical projection tomography. Biomed Opt Express. 2016;7(6):2295–310. https://doi.org/10.1364/BOE.7.002295.

    PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Park S, Kim J, Jeon M, Song J, Kim C. In vivo photoacoustic and fluorescence cystography using clinically relevant dual modal indocyanine green. Sensors (Basel). 2014;14(10):19660–8. https://doi.org/10.3390/s141019660.

    CAS  Article  Google Scholar 

  44. 44.

    Jeon M, Jenkins S, Oh J, Kim J, Peterson T, Chen J, et al. Nonionizing photoacoustic cystography with near-infrared absorbing gold nanostructures as optical-opaque tracers. Nanomedicine. 2014;9(9):1377–88. https://doi.org/10.2217/nnm.13.103.

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Wang LV, Yao J. A practical guide to photoacoustic tomography in the life sciences. Nat Methods. 2016;13(8):627–38. https://doi.org/10.1038/nmeth.3925.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 46.

    Murayama C, Kimura Y, Setou M. Imaging mass spectrometry: principle and application. Biophys Rev. 2009;1(3):131. https://doi.org/10.1007/s12551-009-0015-6.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Bodzon-Kulakowska A, Suder P. Imaging mass spectrometry: instrumentation, applications, and combination with other visualization techniques. Mass Spectrom Rev. 2016;35(1):147–69. https://doi.org/10.1002/mas.21468.

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Sugimoto M, Wakabayashi M, Shimizu Y, Yoshioka T, Higashino K, Numata Y, et al. Imaging mass spectrometry reveals acyl-chain- and region-specific sphingolipid metabolism in the kidneys of sphingomyelin synthase 2-deficient mice. PLoS One. 2016;11(3):e0152191. https://doi.org/10.1371/journal.pone.0152191.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Hong G, Lee JC, Robinson JT, Raaz U, Xie L, Huang NF, et al. Multifunctional in vivo vascular imaging using near-infrared II fluorescence. Nat Med. 2012;18(12):1841–6. https://doi.org/10.1038/nm.2995.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Vahrmeijer AL, Hutteman M, Van Der Vorst JR, Van De Velde CJ, Frangioni JV. Image-guided cancer surgery using near-infrared fluorescence. Nat Rev Clin Oncol. 2013;10(9):507. https://doi.org/10.1038/nrclinonc.2013.123.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Li H, Yao Q, Fan J, Du J, Wang J, Peng X. A two-photon NIR-to-NIR fluorescent probe for imaging hydrogen peroxide in living cells. Biosens Bioelectron. 2017;94:536–43. https://doi.org/10.1016/j.bios.2017.03.039.

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Ciarrocchi E, Belcari N. Cerenkov luminescence imaging: physics principles and potential applications in biomedical sciences. EJNMMI Phys. 2017;4(1):14. https://doi.org/10.1186/s40658-017-0181-8.

    PubMed  PubMed Central  Article  Google Scholar 

  53. 53.

    Timmermand OV, Tran TA, Strand SE, Axelsson J. Intratherapeutic biokinetic measurements, dosimetry parameter estimates, and monitoring of treatment efficacy using Cerenkov luminescence imaging in preclinical radionuclide therapy. J Nucl Med. 2015;56(3):444–9. https://doi.org/10.2967/jnumed.114.148544.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Spinelli AE, Kuo C, Rice BW, Calandrino R, Marzola P, Sbarbati A, et al. Multispectral Cerenkov luminescence tomography for small animal optical imaging. Opt Express. 2011;19(13):12605–18. https://doi.org/10.1364/OE.19.012605.

    CAS  PubMed  Article  Google Scholar 

  55. 55.

    Sahl SJ, Moerner WE. Super-resolution fluorescence imaging with single molecules. Curr Opin Struct Biol. 2013;23(5):778–87. https://doi.org/10.1016/j.sbi.2013.07.010.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Pan D, Hu Z, Qiu F, Huang ZL, Ma Y, Wang Y, et al. A general strategy for developing cell-permeable photo-modulatable organic fluorescent probes for live-cell super-resolution imaging. Nat Commun. 2014;5:5573. https://doi.org/10.1038/ncomms6573.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Sigal YM, Speer CM, Babcock HP, Zhuang X. Mapping synaptic input fields of neurons with super-resolution imaging. Cell. 2015;163(2):493–505. https://doi.org/10.1016/j.cell.2015.08.033.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. 58.

    Townsend DW, Carney JP, Yap JT, Hall NC. PET/CT today and tomorrow. J Nucl Med. 2004;45(Suppl 1):4S–14S.

    PubMed  Google Scholar 

  59. 59.

    Beyer T, Townsend DW, Brun T, Kinahan PE, Charron M, Roddy R, et al. A combined PET/CT scanner for clinical oncology. J Nucl Med. 2000;41(8):1369–79.

    CAS  PubMed  Google Scholar 

  60. 60.

    Farwell MD, Pryma DA, Mankoff DA. PET/CT imaging in cancer: current applications and future directions. Cancer. 2014;120(22):3433–45. https://doi.org/10.1002/cncr.28860.

    CAS  PubMed  Article  Google Scholar 

  61. 61.

    Czernin J, Allen-Auerbach M, Schelbert HR. Improvements in cancer staging with PET/CT: literature-based evidence as of September 2006. J Nucl Med. 2007;48(Suppl 1):78S–88S.

    CAS  PubMed  Google Scholar 

  62. 62.

    UC Davis. Human images from world's first total-body scanner unveiled: 1st-of-its kind scanner to roll out in Sacramento in spring 2019. ScienceDaily. 2018.

  63. 63.

    Lonsdale MN, Beyer T. Dual-modality PET/CT instrumentation-today and tomorrow. Eur J Radiol. 2010;73(3):452–60. https://doi.org/10.1016/j.ejrad.2009.12.021.

    PubMed  Article  Google Scholar 

  64. 64.

    Delso G, Furst S, Jakoby B, Ladebeck R, Ganter C, Nekolla SG, et al. Performance measurements of the Siemens mMR integrated whole-body PET/MR scanner. J Nucl Med. 2011;52(12):1914–22. https://doi.org/10.2967/jnumed.111.092726.

    PubMed  Article  Google Scholar 

  65. 65.

    Boellaard R, Quick HH. Current image acquisition options in PET/MR. Semin Nucl Med. 2015;45(3):192–200. https://doi.org/10.1053/j.semnuclmed.2014.12.001.

    PubMed  Article  Google Scholar 

  66. 66.

    Spick C, Herrmann K, Czernin J. 18F-FDG PET/CT and PET/MRI perform equally well in cancer: evidence from studies on more than 2,300 patients. J Nucl Med. 2016;57(3):420–30. https://doi.org/10.2967/jnumed.115.158808.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  67. 67.

    Civelek AC. (68)Ga-PSMA-11 PET: better at detecting prostate cancer than multiparametric MRI? Radiology. 2018;289(3):738–9. https://doi.org/10.1148/radiol.2018181981.

    PubMed  Article  Google Scholar 

  68. 68.

    Vallabhajosula S, Solnes L, Vallabhajosula B. A broad overview of positron emission tomography radiopharmaceuticals and clinical applications: what is new? Semin Nucl Med. 2011;41(4):246–64. https://doi.org/10.1053/j.semnuclmed.2011.02.003.

    PubMed  Article  Google Scholar 

  69. 69.

    Jiang L, Tu Y, Shi H, Cheng Z. PET probes beyond (18)F-FDG. J Biomed Res. 2014;28(6):435–46. https://doi.org/10.7555/JBR.28.20130196.

    PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Huang T, Civelek AC, Zheng H, Ng CK, Duan X, Li J, et al. 18F-misonidazole PET imaging of hypoxia in micrometastases and macroscopic xenografts of human non-small cell lung cancer: a correlation with autoradiography and histological findings. Am J Nucl Med Mol Imaging. 2013;3(2):142–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Bagheri MH, Ahlman MA, Lindenberg L, Turkbey B, Lin J, Cahid Civelek A, et al. Advances in medical imaging for the diagnosis and management of common genitourinary cancers. Urol Oncol. 2017;35(7):473–91. https://doi.org/10.1016/j.urolonc.2017.04.014.

    PubMed  PubMed Central  Article  Google Scholar 

  72. 72.

    Mallidi S, Luke GP, Emelianov S. Photoacoustic imaging in cancer detection, diagnosis, and treatment guidance. Trends Biotechnol. 2011;29(5):213–21. https://doi.org/10.1016/j.tibtech.2011.01.006.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. 73.

    Zhou M, Tian M, Li C. Copper-based nanomaterials for cancer imaging and therapy. Bioconjug Chem. 2016;27(5):1188–99. https://doi.org/10.1021/acs.bioconjchem.6b00156.

    CAS  PubMed  Article  Google Scholar 

  74. 74.

    Zharov VP. Ultrasharp nonlinear photothermal and photoacoustic resonances and holes beyond the spectral limit. Nat Photonics. 2011;5(2):110–6. https://doi.org/10.1038/nphoton.2010.280.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. 75.

    Wang L, Xia J, Yao J, Maslov KI, Wang LV. Ultrasonically encoded photoacoustic flowgraphy in biological tissue. Phys Rev Lett. 2013;111(20):204301. https://doi.org/10.1103/PhysRevLett.111.204301.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. 76.

    Wang LV, Gao L. Photoacoustic microscopy and computed tomography: from bench to bedside. Annu Rev Biomed Eng. 2014;16:155–85. https://doi.org/10.1146/annurev-bioeng-071813-104553.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    Liu Y, Nie L, Chen X. Photoacoustic molecular imaging: from multiscale biomedical applications towards early-stage theranostics. Trends Biotechnol. 2016;34(5):420–33. https://doi.org/10.1016/j.tibtech.2016.02.001.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

    Wang LV, Hu S. Photoacoustic tomography: in vivo imaging from organelles to organs. Science. 2012;335(6075):1458–62. https://doi.org/10.1126/science.1216210.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79.

    Sussman CB, Rossignol C, Zhang Q, Jiang H, Zheng T, Steindler D, et al. Photoacoustic tomography can detect cerebral hemodynamic alterations in a neonatal rodent model of hypoxia-ischemia. Acta Neurobiol Exp. 2012;72:253–63.

    Google Scholar 

  80. 80.

    Kruger RA, Lam RB, Reinecke DR, Del Rio SP, Doyle RP. Photoacoustic angiography of the breast. Med Phys. 2010;37(11):6096–100. https://doi.org/10.1118/1.3497677.

    PubMed  PubMed Central  Article  Google Scholar 

  81. 81.

    Robinson JT, Hong G, Liang Y, Zhang B, Yaghi OK, Dai H. In vivo fluorescence imaging in the second near-infrared window with long circulating carbon nanotubes capable of ultrahigh tumor uptake. J Am Chem Soc. 2012;134(25):10664–9. https://doi.org/10.1021/ja303737a.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Welsher K, Sherlock SP, Dai H. Deep-tissue anatomical imaging of mice using carbon nanotube fluorophores in the second near-infrared window. Proc Natl Acad Sci U S A. 2011;108(22):8943–8. https://doi.org/10.1073/pnas.1014501108.

    PubMed  PubMed Central  Article  Google Scholar 

  83. 83.

    Ji M, Xu M, Zhang W, Yang Z, Huang L, Liu J, et al. Structurally well-defined Au@Cu2- x S core-shell nanocrystals for improved cancer treatment based on enhanced photothermal efficiency. Adv Mater. 2016;28(16):3094–101. https://doi.org/10.1002/adma.201503201.

    CAS  PubMed  Article  Google Scholar 

  84. 84.

    Hong G, Zou Y, Antaris AL, Diao S, Wu D, Cheng K, et al. Ultrafast fluorescence imaging in vivo with conjugated polymer fluorophores in the second near-infrared window. Nat Commun. 2014;5:4206. https://doi.org/10.1038/ncomms5206.

    CAS  PubMed  Article  Google Scholar 

  85. 85.

    Hell SW. Far-field optical nanoscopy. Science. 2007;316(5828):1153–8. https://doi.org/10.1126/science.1137395.

    CAS  PubMed  Article  Google Scholar 

  86. 86.

    Hell SW, Wichmann J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett. 1994;19(11):780–2. https://doi.org/10.1364/ol.19.000780.

    CAS  PubMed  Article  Google Scholar 

  87. 87.

    Gustafsson MG. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc. 2000;198(2):82–7. https://doi.org/10.1046/j.1365-2818.2000.00710.x.

    CAS  PubMed  Article  Google Scholar 

  88. 88.

    Rust MJ, Bates M, Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods. 2006;3(10):793–5. https://doi.org/10.1038/nmeth929.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. 89.

    Bement WM, Leda M, Moe AM, Kita AM, Larson ME, Golding AE, et al. Activator-inhibitor coupling between Rho signalling and actin assembly makes the cell cortex an excitable medium. Nat Cell Biol. 2015;17(11):1471–83. https://doi.org/10.1038/ncb3251.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. 90.

    Hess ST, Girirajan TP, Mason MD. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J. 2006;91(11):4258–72. https://doi.org/10.1529/biophysj.106.091116.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  91. 91.

    Xu Y, Liu H, Cheng Z. Harnessing the power of radionuclides for optical imaging: Cerenkov luminescence imaging. J Nucl Med. 2011;52(12):2009–18. https://doi.org/10.2967/jnumed.111.092965.

    PubMed  Article  Google Scholar 

  92. 92.

    Tanha K, Pashazadeh AM, Pogue BW. Review of biomedical Cerenkov luminescence imaging applications. Biomed Opt Express. 2015;6(8):3053–65. https://doi.org/10.1364/BOE.6.003053.

    PubMed  PubMed Central  Article  Google Scholar 

  93. 93.

    Xu Y, Chang E, Liu H, Jiang H, Gambhir SS, Cheng Z. Proof-of-concept study of monitoring cancer drug therapy with cerenkov luminescence imaging. J Nucl Med. 2012;53(2):312–7. https://doi.org/10.2967/jnumed.111.094623.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. 94.

    Holland JP, Normand G, Ruggiero A, Lewis JS, Grimm J. Intraoperative imaging of positron emission tomographic radiotracers using Cerenkov luminescence emissions. Mol Imaging. 2011;10(3). https://doi.org/10.2310/7290.2010.00047.

  95. 95.

    Liu H, Carpenter CM, Jiang H, Pratx G, Sun C, Buchin MP, et al. Intraoperative imaging of tumors using Cerenkov luminescence endoscopy: a feasibility experimental study. J Nucl Med. 2012;53(10):1579–84. https://doi.org/10.2967/jnumed.111.098541.

    PubMed  PubMed Central  Article  Google Scholar 

  96. 96.

    Thorek DLJ, Riedl CC, Grimm J. Clinical Cerenkov luminescence imaging of 18F-FDG. J Nucl Med. 2013;55(1):95–8. https://doi.org/10.2967/jnumed.113.127266.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  97. 97.

    Hu H, Cao X, Kang F, Wang M, Lin Y, Liu M, et al. Feasibility study of novel endoscopic Cerenkov luminescence imaging system in detecting and quantifying gastrointestinal disease: first human results. Eur Radiol. 2015;25(6):1814–22. https://doi.org/10.1007/s00330-014-3574-2.

    PubMed  Article  Google Scholar 

  98. 98.

    Spinelli AE, Boschi F. Optimizing in vivo small animal Cerenkov luminescence imaging. J Biomed Opt. 2012;17(4):040506. https://doi.org/10.1117/1.JBO.17.4.040506.

    PubMed  Article  Google Scholar 

  99. 99.

    Ruggiero A, Holland JP, Lewis JS, Grimm J. Cerenkov luminescence imaging of medical isotopes. J Nucl Med. 2010;51(7):1123–30. https://doi.org/10.2967/jnumed.110.076521.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  100. 100.

    Massoud TF, Gambhir SS. Molecular imaging in living subjects: seeing fundamental biological processes in a new light. Genes Dev. 2003;17(5):545–80. https://doi.org/10.1101/gad.1047403.

    CAS  PubMed  Article  Google Scholar 

  101. 101.

    Islam T, Harisinghani MG. Overview of nanoparticle use in cancer imaging. Cancer Biomark. 2009;5(2):61–7. https://doi.org/10.3233/CBM-2009-0578.

    CAS  PubMed  Article  Google Scholar 

  102. 102.

    Padmanabhan P, Kumar A, Kumar S, Chaudhary RK, Gulyas B. Nanoparticles in practice for molecular-imaging applications: An overview. Acta Biomater. 2016;41:1–16. https://doi.org/10.1016/j.actbio.2016.06.003.

    CAS  PubMed  Article  Google Scholar 

  103. 103.

    Jaffer FA, Libby P, Weissleder R. Optical and multimodality molecular imaging: insights into atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29(7):1017–24. https://doi.org/10.1161/ATVBAHA.108.165530.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. 104.

    Xie J, Chen K, Huang J, Lee S, Wang J, Gao J, et al. PET/NIRF/MRI triple functional iron oxide nanoparticles. Biomaterials. 2010;31(11):3016–22. https://doi.org/10.1016/j.biomaterials.2010.01.010.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. 105.

    Hu H, Huang P, Weiss OJ, Yan X, Yue X, Zhang MG, et al. PET and NIR optical imaging using self-illuminating (64)Cu-doped chelator-free gold nanoclusters. Biomaterials. 2014;35(37):9868–76. https://doi.org/10.1016/j.biomaterials.2014.08.038.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. 106.

    Locke LW, Mayo MW, Yoo AD, Williams MB, Berr SS. PET imaging of tumor associated macrophages using mannose coated 64Cu liposomes. Biomaterials. 2012;33(31):7785–93. https://doi.org/10.1016/j.biomaterials.2012.07.022.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  107. 107.

    Keliher EJ, Yoo J, Nahrendorf M, Lewis JS, Marinelli B, Newton A, et al. 89Zr-labeled dextran nanoparticles allow in vivo macrophage imaging. Bioconjug Chem. 2011;22(12):2383–9. https://doi.org/10.1021/bc200405d.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  108. 108.

    Ruggiero A, Villa CH, Holland JP, Sprinkle SR, May C, Lewis JS, et al. Imaging and treating tumor vasculature with targeted radiolabeled carbon nanotubes. Int J Nanomedicine. 2010;5:783–802. https://doi.org/10.2147/IJN.S13300.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. 109.

    Thorek DL, Ulmert D, Diop NF, Lupu ME, Doran MG, Huang R, et al. Non-invasive mapping of deep-tissue lymph nodes in live animals using a multimodal PET/MRI nanoparticle. Nat Commun. 2014;5:3097. https://doi.org/10.1038/ncomms4097.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  110. 110.

    Karmani L, Labar D, Valembois V, Bouchat V, Nagaswaran PG, Bol A, et al. Antibody-functionalized nanoparticles for imaging cancer: influence of conjugation to gold nanoparticles on the biodistribution of89Zr-labeled cetuximab in mice. Contrast Media Mol Imaging. 2013;8(5):402–8. https://doi.org/10.1002/cmmi.1539.

    CAS  PubMed  Article  Google Scholar 

  111. 111.

    Karmani L, Bouchat V, Bouzin C, Levêque P, Labar D, Bol A, et al. 89Zr-labeled anti-endoglin antibody-targeted gold nanoparticles for imaging cancer: implications for future cancer therapy. Nanomedicine. 2014;9(13):1923–37.

    CAS  PubMed  Article  Google Scholar 

  112. 112.

    Park JC, Yu MK, An GI, Park SI, Oh J, Kim HJ, et al. Facile preparation of a hybrid nanoprobe for triple-modality optical/PET/MR imaging. Small. 2010;6(24):2863–8. https://doi.org/10.1002/smll.201001418.

    CAS  PubMed  Article  Google Scholar 

  113. 113.

    Kim J, Pandya DN, Lee W, Park JW, Kim YJ, Kwak W, et al. Vivid Tumor imaging utilizing liposome-carried bimodal radiotracer. ACS Med Chem Lett. 2014;5(4):390–4. https://doi.org/10.1021/ml400513g.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. 114.

    Benezra M, Penate-Medina O, Zanzonico PB, Schaer D, Ow H, Burns A, et al. Multimodal silica nanoparticles are effective cancer-targeted probes in a model of human melanoma. J Clin Invest. 2011;121(7):2768–80. https://doi.org/10.1172/jci45600.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. 115.

    Yang BY, Moon SH, Seelam SR, Jeon MJ, Lee YS, Lee DS, et al. Development of a multimodal imaging probe by encapsulating iron oxide nanoparticles with functionalized amphiphiles for lymph node imaging. Nanomedicine. 2015;10(12):1899–910. https://doi.org/10.2217/nnm.15.41.

    CAS  PubMed  Article  Google Scholar 

  116. 116.

    Madru R, Tran TA, Axelsson J, Ingvar C, Bibic A, Ståhlberg F, et al. 68Ga-labeled superparamagnetic iron oxide nanoparticles (SPIONs) for multi-modality PET/MR/Cherenkov luminescence imaging of sentinel lymph nodes. Am J Nucl Med Mol Imaging. 2014;4(1):60–9.

    CAS  Google Scholar 

  117. 117.

    Su T, Wang YB, Han D, Wang J, Qi S, Gao L, et al. Multimodality Imaging of angiogenesis in a rabbit atherosclerotic model by GEBP11 peptide targeted nanoparticles. Theranostics. 2017;7(19):4791–804. https://doi.org/10.7150/thno.20767.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  118. 118.

    Kim SM, Chae MK, Yim MS, Jeong IH, Cho J, Lee C, et al. Hybrid PET/MR imaging of tumors using an oleanolic acid-conjugated nanoparticle. Biomaterials. 2013;34(33):8114–21. https://doi.org/10.1016/j.biomaterials.2013.07.078.

    CAS  PubMed  Article  Google Scholar 

  119. 119.

    Doughton JA, Hofman MS, Eu P, Hicks RJ, Williams S. A first-in-human study of (68)Ga-nanocolloid PET/CT sentinel lymph node imaging in prostate cancer demonstrates aberrant lymphatic drainage pathways. J Nucl Med. 2018;59(12):1837–42. https://doi.org/10.2967/jnumed.118.209171.

    CAS  PubMed  Article  Google Scholar 

  120. 120.

    Lamichhane N, Shen KW, Li CL, Han QX, Zhang YJ, Shao ZM, et al. Sentinel lymph node biopsy in breast cancer patients after overnight migration of radiolabelled sulphur colloid. Postgrad Med J. 2004;80(947):546–50. https://doi.org/10.1136/pgmj.2003.016311.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  121. 121.

    Nelson KP, Choudhury KR, Coleman RE, Shipes SW, Siler WL, Hubble WL, et al. Does the preparation and utilization of 99mTc-sulfur colloid affect the outcomes of breast lymphoscintigraphy? J Nucl Med Technol. 2013;41(2):92–8. https://doi.org/10.2967/jnmt.112.117820.

    PubMed  Article  Google Scholar 

  122. 122.

    Gommans GM, van Dongen A, van der Schors TG, Gommans E, Visser JF, Clarijs WW, et al. Further optimisation of 99mTc-nanocoll sentinel node localisation in carcinoma of the breast by improved labelling. Eur J Nucl Med. 2001;28(10):1450–5. https://doi.org/10.1007/s002590100590.

    CAS  PubMed  Article  Google Scholar 

  123. 123.

    Jimenez-Mancilla N, Ferro-Flores G, Santos-Cuevas C, Ocampo-Garcia B, Luna-Gutierrez M, Azorin-Vega E, et al. Multifunctional targeted therapy system based on (99 m) Tc/(177) Lu-labeled gold nanoparticles-Tat(49-57)-Lys(3)-bombesin internalized in nuclei of prostate cancer cells. J Labelled Comp Radiopharm. 2013;56(13):663–71. https://doi.org/10.1002/jlcr.3087.

    CAS  PubMed  Article  Google Scholar 

  124. 124.

    Morales-Avila E, Ferro-Flores G, Ocampo-Garcia BE, De Leon-Rodriguez LM, Santos-Cuevas CL, Garcia-Becerra R, et al. Multimeric system of 99mTc-labeled gold nanoparticles conjugated to c[RGDfK(C)] for molecular imaging of tumor alpha(v)beta(3) expression. Bioconjug Chem. 2011;22(5):913–22. https://doi.org/10.1021/bc100551s.

    CAS  PubMed  Article  Google Scholar 

  125. 125.

    Torres Martin de Rosales R, Tavare R, Glaria A, Varma G, Protti A, Blower PJ. (99 m)Tc-bisphosphonate-iron oxide nanoparticle conjugates for dual-modality biomedical imaging. Bioconjug Chem. 2011;22(3):455–65. https://doi.org/10.1021/bc100483k.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. 126.

    Khosroshahi A, Amanlou M, Sabzevari O, Daha F, Aghasadeghi M, Ghorbani M, et al. A comparative study of two novel nanosized radiolabeled analogues of methionine for SPECT tumor imaging. Curr Med Chem. 2013;20(1):123–33.

    CAS  PubMed  Article  Google Scholar 

  127. 127.

    Awasthi V, Goins B, McManus L, Klipper R, Phillipsa WT. [99mTc] liposomes for localizing experimental colitis in a rabbit model. Nucl Med Biol. 2003;30(2):159–68. https://doi.org/10.1016/s0969-8051(02)00419-5.

    CAS  PubMed  Article  Google Scholar 

  128. 128.

    Oyen WJ, Boerman OC, Storm G. Bloois Lv, Koenders EB, Claessens RA et al. Detecting infection and inflammation with technetium-99 m-labeled Stealth liposomes. J Nucl Med. 1996;37(8):1392–7.

    CAS  PubMed  Google Scholar 

  129. 129.

    Zhang G, Yang Z, Lu W, Zhang R, Huang Q, Tian M, et al. Influence of anchoring ligands and particle size on the colloidal stability and in vivo biodistribution of polyethylene glycol-coated gold nanoparticles in tumor-xenografted mice. Biomaterials. 2009;30(10):1928–36. https://doi.org/10.1016/j.biomaterials.2008.12.038.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  130. 130.

    Ogawa M, Umeda IO, Kosugi M, Kawai A, Hamaya Y, Takashima M, et al. Development of 111In-labeled liposomes for vulnerable atherosclerotic plaque imaging. J Nucl Med. 2014;55(1):115–20. https://doi.org/10.2967/jnumed.113.123158.

    CAS  PubMed  Article  Google Scholar 

  131. 131.

    Boerman OC, Storm G, Oyen WJ. Bloois Lv, van der Meer JW, Claessens RA et al. Sterically stabilized liposomes labeled with indium-111 to image focal infection. J Nucl Med. 1995;36(9):1639–44.

    CAS  PubMed  Google Scholar 

  132. 132.

    de Vries A, Kok MB, Sanders HM, Nicolay K, Strijkers GJ, Grull H. Multimodal liposomes for SPECT/MR imaging as a tool for in situ relaxivity measurements. Contrast Media Mol Imaging. 2012;7(1):68–75. https://doi.org/10.1002/cmmi.468.

    CAS  PubMed  Article  Google Scholar 

  133. 133.

    Strijkers GJ, Mulder WJ, van Heeswijk RB, Frederik PM, Bomans P, Magusin PC, et al. Relaxivity of liposomal paramagnetic MRI contrast agents. MAGMA. 2005;18(4):186–92. https://doi.org/10.1007/s10334-005-0111-y.

    CAS  PubMed  Article  Google Scholar 

  134. 134.

    Dong C, Korinek A, Blasiak B, Tomanek B, van Veggel FCJM. Cation exchange: a facile method to make NaYF4:Yb,Tm-NaGdF4 core–shell nanoparticles with a thin, tunable, and uniform shell. Chem Mater. 2012;24(7):1297–305. https://doi.org/10.1021/cm2036844.

    CAS  Article  Google Scholar 

  135. 135.

    Anishur Rahman AT, Majewski P, Vasilev K. Gd2O3 nanoparticles: size-dependent nuclear magnetic resonance. Contrast Media Mol Imaging. 2013;8(1):92–5. https://doi.org/10.1002/cmmi.1481.

    CAS  PubMed  Article  Google Scholar 

  136. 136.

    Bridot JL, Faure AC, Laurent S, Riviere C, Billotey C, Hiba B, et al. Hybrid gadolinium oxide nanoparticles: multimodal contrast agents for in vivo imaging. J Am Chem Soc. 2007;129(16):5076–84. https://doi.org/10.1021/ja068356j.

    CAS  PubMed  Article  Google Scholar 

  137. 137.

    Park JY, Baek MJ, Choi ES, Woo S, Kim JH, Kim TJ, et al. Paramagnetic ultrasmall gadolinium oxide nanoparticles as advanced T 1 MRI contrast agent: account for large longitudinal relaxivity, optimal particle diameter, and in vivo T 1 MR images. ACS Nano. 2009;3(11):3663–9. https://doi.org/10.1021/nn900761s.

    CAS  PubMed  Article  Google Scholar 

  138. 138.

    Bulte JW, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 2004;17(7):484–99. https://doi.org/10.1002/nbm.924.

    CAS  PubMed  Article  Google Scholar 

  139. 139.

    Kim T, Cho EJ, Chae Y, Kim M, Oh A, Jin J, et al. Urchin-shaped manganese oxide nanoparticles as pH-responsive activatable T1 contrast agents for magnetic resonance imaging. Angew Chem Int Ed Eng. 2011;50(45):10589–93. https://doi.org/10.1002/anie.201103108.

    CAS  Article  Google Scholar 

  140. 140.

    Kim BH, Lee N, Kim H, An K, Park YI, Choi Y, et al. Large-scale synthesis of uniform and extremely small-sized iron oxide nanoparticles for high-resolution T1 magnetic resonance imaging contrast agents. J Am Chem Soc. 2011;133(32):12624–31. https://doi.org/10.1021/ja203340u.

    CAS  PubMed  Article  Google Scholar 

  141. 141.

    Tong S, Hou S, Zheng Z, Zhou J, Bao G. Coating optimization of superparamagnetic iron oxide nanoparticles for high T2 relaxivity. Nano Lett. 2010;10(11):4607–13. https://doi.org/10.1021/nl102623x.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  142. 142.

    Park JH, von Maltzahn G, Zhang L, Schwartz MP, Ruoslahti E, Bhatia SN, et al. Magnetic iron oxide nanoworms for tumor targeting and imaging. Adv Mater. 2008;20(9):1630–5. https://doi.org/10.1002/adma.200800004.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  143. 143.

    De La Zerda A, Zavaleta C, Keren S, Vaithilingam S, Bodapati S, Liu Z, et al. Carbon nanotubes as photoacoustic molecular imaging agents in living mice. Nat Nanotechnol. 2008;3(9):557–62. https://doi.org/10.1038/nnano.2008.231.

    CAS  PubMed  Article  Google Scholar 

  144. 144.

    Ku G, Zhou M, Song S, Huang Q, Hazle J, Li C. Copper sulfide nanoparticles as a new class of photoacoustic contrast agent for deep tissue imaging at 1064 nm. ACS Nano. 2012;6(8):7489–96. https://doi.org/10.1021/nn302782y.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  145. 145.

    Zhou M, Ku G, Pageon L, Li C. Theranostic probe for simultaneous in vivo photoacoustic imaging and confined photothermolysis by pulsed laser at 1064 nm in 4 T1 breast cancer model. Nanoscale. 2014;6(24):15228–35. https://doi.org/10.1039/c4nr05386a.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  146. 146.

    Jokerst JV, Thangaraj M, Kempen PJ, Sinclair R, Gambhir SS. Photoacoustic imaging of mesenchymal stem cells in living mice via silica-coated gold nanorods. ACS Nano. 2012;6(7):5920–30. https://doi.org/10.1021/nn302042y.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  147. 147.

    Li PC, Wang C-RC, Shieh DB, Wei CW, Liao CK, Poe C, et al. In vivo photoacoustic molecular imaging with simultaneous multiple selective targeting using antibody-conjugated gold nanorods. Opt Express. 2008;16(23):18605–15. https://doi.org/10.1364/oe.16.018605.

    CAS  PubMed  Article  Google Scholar 

  148. 148.

    Lu W, Huang Q, Ku G, Wen X, Zhou M, Guzatov D, et al. Photoacoustic imaging of living mouse brain vasculature using hollow gold nanospheres. Biomaterials. 2010;31(9):2617–26. https://doi.org/10.1016/j.biomaterials.2009.12.007.

    CAS  PubMed  Article  Google Scholar 

  149. 149.

    Zhou M, Singhana B, Liu Y, Huang Q, Mitcham T, Wallace MJ, et al. Photoacoustic- and magnetic resonance-guided photothermal therapy and tumor vasculature visualization using theranostic magnetic gold nanoshells. J Biomed Nanotechnol. 2015;11(8):1442–50. https://doi.org/10.1166/jbn.2015.2089.

    CAS  PubMed  Article  Google Scholar 

  150. 150.

    Kim S, Lim YT, Soltesz EG, De Grand AM, Lee J, Nakayama A, et al. Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping. Nat Biotechnol. 2004;22(1):93–7. https://doi.org/10.1038/nbt920.

    PubMed  Article  Google Scholar 

  151. 151.

    Hong G, Robinson JT, Zhang Y, Diao S, Antaris AL, Wang Q, et al. In vivo fluorescence imaging with Ag2S quantum dots in the second near-infrared region. Angew Chem Int Ed Eng. 2012;51(39):9818–21.

    CAS  Article  Google Scholar 

  152. 152.

    Du Y, Xu B, Fu T, Cai M, Li F, Zhang Y, et al. Near-infrared photoluminescent Ag2S quantum dots from a single source precursor. J Am Chem Soc. 2010;132(5):1470–1.

    CAS  PubMed  Article  Google Scholar 

  153. 153.

    Larson DR, Ow H, Vishwasrao HD, Heikal AA, Wiesner U, Webb WW. Silica nanoparticle architecture determines radiative properties of encapsulated fluorophores. Chem Mater. 2008;20(8):2677–84. https://doi.org/10.1021/cm7026866.

    CAS  Article  Google Scholar 

  154. 154.

    Francolon N, Boyer D, Leccia F, Jouberton E, Walter A, Bordeianu C, et al. Preparation of core/shell NaYF 4 :Yb,Tm@dendrons nanoparticles with enhanced upconversion luminescence for in vivo imaging. Nanomedicine. 2016;12(7):2107–13. https://doi.org/10.1016/j.nano.2016.05.020.

    CAS  PubMed  Article  Google Scholar 

  155. 155.

    Liu J, Liu Y, Bu W, Bu J, Sun Y, Du J, et al. Ultrasensitive nanosensors based on upconversion nanoparticles for selective hypoxia imaging in vivo upon near-infrared excitation. J Am Chem Soc. 2014;136(27):9701–9. https://doi.org/10.1021/ja5042989.

    CAS  PubMed  Article  Google Scholar 

  156. 156.

    Yang Y, Shao Q, Deng R, Wang C, Teng X, Cheng K, et al. In vitro and in vivo uncaging and bioluminescence imaging by using photocaged upconversion nanoparticles. Angew Chem Int Ed Eng. 2012;51(13):3125–9. https://doi.org/10.1002/anie.201107919.

    CAS  Article  Google Scholar 

  157. 157.

    Hoyer P, Staudt T, Engelhardt J, Hell SW. Quantum dot blueing and blinking enables fluorescence nanoscopy. Nano Lett. 2011;11(1):245–50. https://doi.org/10.1021/nl103639f.

    CAS  PubMed  Article  Google Scholar 

  158. 158.

    Xu J, Tehrani KF, Kner P. Multicolor 3D super-resolution imaging by quantum dot stochastic optical reconstruction microscopy. ACS Nano. 2015;9(3):2917–25.

    CAS  PubMed  Article  Google Scholar 

  159. 159.

    Hanne J, Falk HJ, Gorlitz F, Hoyer P, Engelhardt J, Sahl SJ, et al. STED nanoscopy with fluorescent quantum dots. Nat Commun. 2015;6:7127. https://doi.org/10.1038/ncomms8127.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  160. 160.

    Dertinger T, Colyer R, Iyer G, Weiss S, Enderlein J. Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI). Proc Natl Acad Sci U S A. 2009;106(52):22287–92.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  161. 161.

    Zeng Z, Chen X, Wang H, Huang N, Shan C, Zhang H, et al. Fast super-resolution imaging with ultra-high labeling density achieved by joint tagging super-resolution optical fluctuation imaging. Sci Rep. 2015;5(1):8359. https://doi.org/10.1038/srep08359.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  162. 162.

    Chen X, Zong W, Li R, Zeng Z, Zhao J, Xi P, et al. Two-photon light-sheet nanoscopy by fluorescence fluctuation correlation analysis. Nanoscale. 2016;8(19):9982–7. https://doi.org/10.1039/c6nr00324a.

    CAS  PubMed  Article  Google Scholar 

  163. 163.

    Chen X, Li R, Liu Z, Sun K, Sun Z, Chen D, et al. Small photoblinking semiconductor polymer dots for fluorescence nanoscopy. Adv Mater. 2017;29(5). https://doi.org/10.1002/adma.201604850.

  164. 164.

    Abou DS, Pickett JE, Thorek DL. Nuclear molecular imaging with nanoparticles: radiochemistry, applications and translation. Br J Radiol. 2015;88(1054):20150185. https://doi.org/10.1259/bjr.20150185.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  165. 165.

    Nahrendorf M, Zhang H, Hembrador S, Panizzi P, Sosnovik DE, Aikawa E, et al. Nanoparticle PET-CT imaging of macrophages in inflammatory atherosclerosis. Circulation. 2008;117(3):379–87. https://doi.org/10.1161/circulationaha.107.741181.

    CAS  PubMed  Article  Google Scholar 

  166. 166.

    Phillips E, Penate-Medina O, Zanzonico PB, Carvajal RD, Mohan P, Ye Y, et al. Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Sci Transl Med. 2014;6(260):260ra149. https://doi.org/10.1126/scitranslmed.3009524.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  167. 167.

    Fang J, Chandrasekharan P, Liu XL, Yang Y, Lv YB, Yang CT, et al. Manipulating the surface coating of ultra-small Gd2O3 nanoparticles for improved T1-weighted MR imaging. Biomaterials. 2014;35(5):1636–42. https://doi.org/10.1016/j.biomaterials.2013.11.032.

    CAS  PubMed  Article  Google Scholar 

  168. 168.

    Zeng J, Jing L, Hou Y, Jiao M, Qiao R, Jia Q, et al. Anchoring group effects of surface ligands on magnetic properties of Fe(3) O(4) nanoparticles: towards high performance MRI contrast agents. Adv Mater. 2014;26(17):2694–8. https://doi.org/10.1002/adma.201304744.

    CAS  PubMed  Article  Google Scholar 

  169. 169.

    Na HB, Lee JH, An K, Park YI, Park M, Lee IS, et al. Development of a T1 Contrast Agent for Magnetic Resonance Imaging Using MnO Nanoparticles. Angew Chem Int Ed Eng. 2007;46(28):5397–401. https://doi.org/10.1002/anie.200604775.

    CAS  Article  Google Scholar 

  170. 170.

    Wang X, Pang Y, Ku G, Xie X, Stoica G, Wang LV. Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain. Nat Biotechnol. 2003;21(7):803–6. https://doi.org/10.1038/nbt839.

    CAS  PubMed  Article  Google Scholar 

  171. 171.

    Qin C, Cheng K, Chen K, Hu X, Liu Y, Lan X, et al. Tyrosinase as a multifunctional reporter gene for Photoacoustic/MRI/PET triple modality molecular imaging. Sci Rep. 2013;3:1490. https://doi.org/10.1038/srep01490.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  172. 172.

    Wang Y, Xie X, Wang X, Ku G, Gill KL, O'Neal DP, et al. Photoacoustic tomography of a nanoshell contrast agent in the in vivo rat brain. Nano Lett. 2004;4(9):1689–92. https://doi.org/10.1021/nl072349r.

    CAS  Article  Google Scholar 

  173. 173.

    Hilderbrand SA, Weissleder R. Near-infrared fluorescence: application to in vivo molecular imaging. Curr Opin Chem Biol. 2010;14(1):71–9. https://doi.org/10.1016/j.cbpa.2009.09.029.

    CAS  PubMed  Article  Google Scholar 

  174. 174.

    Yang L, Peng XH, Wang YA, Wang X, Cao Z, Ni C, et al. Receptor-targeted nanoparticles for in vivo imaging of breast cancer. Clin Cancer Res. 2009;15(14):4722–32. https://doi.org/10.1158/1078-0432.Ccr-08-3289.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  175. 175.

    Li X, Huang T, Jiang H, Wang X, Shen B, Wang X, et al. Combined injection of 18F-fluorodeoxyglucose and 3'-deoxy-3'-[18F] fluorothymidine PET achieves more complete identification of viable lung cancer cells in mice and patients than individual radiopharmaceutical: a proof-of-concept study. Transl Oncol. 2013;6(6):775. https://doi.org/10.1593/tlo.13577.

    PubMed  PubMed Central  Article  Google Scholar 

  176. 176.

    Hosny A, Parmar C, Quackenbush J, Schwartz LH, Aerts HJWL. Artificial intelligence in radiology. Nat Rev Cancer. 2018;18(8):500–10. https://doi.org/10.1038/s41568-018-0016-5.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Funding

This work was funded by the grants from the National Key Research and the Development Program of China (no. 2016YFA0100900), the National Natural Science Foundation of China (NSFC) (no. 81725009, 81761148029, 21788102, 81900255, 82030049), and the Fundamental Research Funds for the Central Universities (2020FZZX001-05).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Yasuyoshi Watanabe or Mei Tian or Hong Zhang.

Ethics declarations

The funding sources had no role in the design or conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Letter to the Editor.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, K., Sun, Y., Wu, S. et al. Systematic imaging in medicine: a comprehensive review. Eur J Nucl Med Mol Imaging (2020). https://doi.org/10.1007/s00259-020-05107-z

Download citation

Keywords

  • Systematic imaging
  • Multimodality
  • Nanoparticle
  • Imaging agent
  • Artificial intelligence